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Epigenetics and pulmonary diseases in the horizon of precision medicine: a review

Giuditta Benincasa, Dawn L. DeMeo, Kimberly Glass, Edwin K. Silverman, Claudio Napoli
European Respiratory Journal 2021 57: 2003406; DOI: 10.1183/13993003.03406-2020
Giuditta Benincasa
1Dept of Advanced Medical and Surgical Sciences (DAMSS), University of Campania “Luigi Vanvitelli”, Naples, Italy
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Dawn L. DeMeo
2Channing Division of Network Medicine and the Division of Pulmonary and Critical Care Medicine, Dept of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
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Kimberly Glass
2Channing Division of Network Medicine and the Division of Pulmonary and Critical Care Medicine, Dept of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
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Edwin K. Silverman
2Channing Division of Network Medicine and the Division of Pulmonary and Critical Care Medicine, Dept of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
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Claudio Napoli
1Dept of Advanced Medical and Surgical Sciences (DAMSS), University of Campania “Luigi Vanvitelli”, Naples, Italy
3Clinical Dept of Internal and Specialty Medicine (DAI), University Hospital (AOU), University of Campania “Luigi Vanvitelli”, Naples, Italy
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Abstract

Epigenetic mechanisms represent potential molecular routes which could bridge the gap between genetic background and environmental risk factors contributing to the pathogenesis of pulmonary diseases. In patients with COPD, asthma and pulmonary arterial hypertension (PAH), there is emerging evidence of aberrant epigenetic marks, mainly including DNA methylation and histone modifications which directly mediate reversible modifications to the DNA without affecting the genomic sequence. Post-translational events and microRNAs can be also regulated epigenetically and potentially participate in disease pathogenesis. Thus, novel pathogenic mechanisms and putative biomarkers may be detectable in peripheral blood, sputum, nasal and buccal swabs or lung tissue. Besides, DNA methylation plays an important role during the early phases of fetal development and may be impacted by environmental exposures, ultimately influencing an individual's susceptibility to COPD, asthma and PAH later in life. With the advances in omics platforms and the application of computational biology tools, modelling the epigenetic variability in a network framework, rather than as single molecular defects, provides insights into the possible molecular pathways underlying the pathogenesis of COPD, asthma and PAH. Epigenetic modifications may have clinical applications as noninvasive biomarkers of pulmonary diseases. Moreover, combining molecular assays with network analysis of epigenomic data may aid in clarifying the multistage transition from a “pre-disease” to “disease” state, with the goal of improving primary prevention of lung diseases and its subsequent clinical management.

We describe epigenetic mechanisms known to be associated with pulmonary diseases and discuss how network analysis could improve our understanding of lung diseases.

Abstract

Network medicine approaches, supporting the integrative analysis of global epigenetic changes, clinical features and environmental factors, provide new hypotheses for pathogenesis of chronic lung diseases and lead to new interventions for prevention https://bit.ly/3kHND9m

Footnotes

  • This article has supplementary material available from erj.ersjournals.com

  • Author contributions: G. Benincasa, D.L. DeMeo, E.K. Silverman and C. Napoli contributed to the study concept and design. G. Benincasa, D.L. DeMeo, K. Glass, E.K. Silverman and C. Napoli contributed to acquisition, analysis, or interpretation of data. G. Benincasa, D.L. DeMeo and K. Glass drafted the manuscript. G. Benincasa, D.L. DeMeo and C. Napoli did critical revision of the manuscript for important intellectual content. G. Benincasa prepared the figures.

  • Conflict of interest: G. Benincasa has nothing to disclose.

  • Conflict of interest: D.L. DeMeo has nothing to disclose.

  • Conflict of interest: K. Glass has nothing to disclose.

  • Conflict of interest: E.K. Silverman has nothing to disclose.

  • Conflict of interest: C. Napoli has nothing to disclose.

  • Support statement: This manuscript was funded by National Research Competitive Grant (PRIN supporting grant no. F8ZB89) from Ministry for University and Research, Italy (to C. Napoli). G. Benincasa is a PhD Student in Translational Medicine supported from University of Campania “Luigi Vanvitelli,” Naples, Italy. This study was also funded by US National Institutes of Health grants U01 HL089856, P01 HL114501, P01 HL132825, R01 HL147148, R01 HL133135, R01 HL137927 and K25 HL133599. E.K. Silverman reports institutional grant funding from GSK and Bayer. D.L. DeMeo reports institutional grant funding from Bayer and a research grant from the Alpha-1 Foundation. Funding information for this article has been deposited with the Crossref Funder Registry.

  • Received September 6, 2020.
  • Accepted November 10, 2020.
  • Copyright ©ERS 2021
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Vol 57 Issue 6 Table of Contents
European Respiratory Journal: 57 (6)
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Epigenetics and pulmonary diseases in the horizon of precision medicine: a review
Giuditta Benincasa, Dawn L. DeMeo, Kimberly Glass, Edwin K. Silverman, Claudio Napoli
European Respiratory Journal Jun 2021, 57 (6) 2003406; DOI: 10.1183/13993003.03406-2020

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Epigenetics and pulmonary diseases in the horizon of precision medicine: a review
Giuditta Benincasa, Dawn L. DeMeo, Kimberly Glass, Edwin K. Silverman, Claudio Napoli
European Respiratory Journal Jun 2021, 57 (6) 2003406; DOI: 10.1183/13993003.03406-2020
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  • Article
    • Abstract
    • Abstract
    • Introduction
    • A focus on molecular basis of epigenetic mechanisms
    • Network medicine and pulmonary diseases
    • The proposed hypothesis of “fetal origins” of pulmonary diseases: epigenetics for primary prevention?
    • Differential epigenetic biomarkers for prevention of pulmonary diseases in post-natal life
    • Network approaches to modelling epigenetic variability in primary prevention of pulmonary diseases
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